Botanischer Centralblatt. A third very useful application of parthenogenesis in plant breeding is the potential to link diploid with polyploid gene pools, in alternation with apomeiosis. The one-domain ERF-like genes typically are involved in biotic or abiotic stress response whereas the two-domain AP2-like genes function in growth and development (Floyd and Bowman, 2007). The recognition that some plant species are capable of asexual reproduction came only two decades after the universality of “the law of sexual reproduction” was established, realizing that this also holds for plants (c. 1830) (Nogler, 2007). Genetic separation of autonomous endosperm formation (AutE) from two other components of apomixis in Hieracium. Sterile haploids also were derived through parthenogenesis of reduced egg cells in rice and maize (Conner et al., 2017). (2016). RBR1 in plants functions in cell cycle control during gametogenesis, with mutants showing supernumerary nuclei at the micropylar end and impaired cellularization (Johnston et al., 2008, 2010). Digonnet, C., Aldon, D., Leduc, N., Dumas, C., and Rougier, M. (1997). Development 124, 2867–2874. Plant J. 54, 656–665. Proc. They are mentioned here for completeness, but we refer to the other reviews for their listing and details, since a specific role in parthenogenesis is yet undetermined. (2010). They are the most resistant to unfavourable conditions of environment, and are able, by a process of parthenogenesis, to give rise to ordinary, indifferent forms again, which can repopulate the gnat. This shows parallelisms to an artificially induced case of parthenogenesis in mice through the loss of distal DNA methylation, resulting in maternal activation of the paternally expressed Insulin-like growth factor 2 (Igf2) gene (Kono et al., 2004). doi: 10.1038/sj.hdy.6800808, Baroux, C., and Grossniklaus, U. RNA interference is essential for cellular quiescence. Zeitschr. Different PRC2s exist, with the one involved in seed development containing the fertilization independent seed (FIS)-class proteins: MEDEA (MEA) (Grossniklaus et al., 1998), FIS2 (Luo et al., 1999), FERTILIZATION-INDEPENDENT ENDOSPERM (FIE) (Ohad et al., 1999), and MULTICOPY SUPPRESSOR OF IRA1 (MSI1) (Köhler et al., 2003a). Several evidences suggest that embryogenesis in plants also mainly relies on maternal transcripts (Autran et al., 2011), although paternal contribution soon after fertilization is also reported (Del Toro-De León et al., 2014; Anderson et al., 2017), and hypothesized to trigger embryogenesis of fertilized egg cells (Khanday et al., 2018). The maternal-to-Zygotic transition in flowering plants: evidence, mechanisms, and plasticity. Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Synthetic clonal reproduction through seeds. J. Exp. Rövekamp, M., Bowman, J. L., and Grossniklaus, U. Plant Sci. Figure 2. 6, 285–296. doi: 10.1242/dev.134668, Islam, S. M., and Tuteja, N. (2012). Parthenogenesis definition is - reproduction by development of an unfertilized usually female gamete that occurs especially among lower plants and invertebrate animals. doi: 10.1007/BF00985373, Noyes, R. D. (2005). Blacktip sharks can reproduce both sexually and asexually. Mutations in one of the FIS-class genes result in autonomous endosperm formation, showing diploid nuclei and development until cellularization (Chaudhury et al., 1997). A., Mookkan, M., Huo, H., Chae, K., and Ozias-Akins, P. (2015). All type-A triploids and the diploid hybrids gave rise to diploid offspring only after pollination with haploid pollen, suggesting that they were true sexuals. Radoeva, T., and Weijers, D. (2014). PO-A and MS gave valuable review comments. The phenomenon is rarer among plants (where it is called parthenocarpy) than among animals. (2004). Plant germline formation: common concepts and developmental flexibility in sexual and asexual reproduction. Plant Cell doi: 10.1105/tpc.18.00518 [Epub ahead of print]. Plant Biol. In vitro protocols for DH-production make use of external stimuli such as a change in ion concentration or other abiotic stress factors to induce embryogenesis in micro- and megaspores (Germanà, 2006; Belogradova et al., 2009; Islam and Tuteja, 2012; Hand et al., 2016). 50, 133–154. Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Embryos obtained with PsASGR-BBML also need either embryo rescue or fertilization of the central cell in order to allow endosperm development and embryo growth progression. Bot. 5. The different forms of embryogenesis are summarized in Figure 1. Particularly the inactivation or modification of the FIS-PRC2 may play a role in these changes. Members of the RKD transcription factor family induce an egg cell-like gene expression program. Radoeva, T., Lokerse, A. S., Llavata-Peris, C. I., Wendrich, J., Xiang, D., Liao, C. Y., et al. A relationship between asexual seed production and either annual plants or monoecious species has also been suggested (among the early investigators: Spallanzani, L., c. 1770–1785, Bernhardi, J., c. 1834–1839, Lecoq, H., c. 1858–1867, and Naudin, C., c. 1861–1867; see Bergsma, 1857). Parthenogenesis characterizes the reproduction of many insects, as aphids or plant-lice. Similar mechanisms of apomeiosis exist in parthenogenetic animals, although here more often meiosis still occurs, involving either haploid offspring or restoration of diploidy through various mechanisms (Avise, 2008). Development 142, 229–241. These observations confirmed the function of a parthenogenesis gene on the basis of its presence and expression in the egg cell, rather than the companion central cell and/or surrounding sporophytic tissue. In a follow-up, Noyes et al. All three aims contribute to the control of plant reproduction and breeding and are highly relevant in order to optimize crop development and increase plant productivity. It also shows the importance of genes involved in the suppression of transcription and modifications thereof at one hand, and in embryogenesis for which transcription is allowed or artificially overexpressed on the other, in parthenogenetic reproduction. U.S.A. 94, 4223–4228. Sex. This method is now awaiting improvements to produce unreduced gametes at high frequency as well as identify or produce CENH3-Like variants in crops. Acad. Ochatt, S. J., Atif, R. M., Patat-Ochatt, E. M., Jacas, L., and Conreux, C. (2010). Parthenogenesis has also been observed in some snakes, fish, and monitor lizards. Crosses between sexual and apomictic dandelions (Taraxacum). In angiosperms, one of two types of apomeiosis (apo = without) occur: apospory, in which the gametophyte develops directly from a sporophytic cell of the ovule, or diplospory, in which meiosis is omitted, restituted, or preceded by endoreplication in the megaspore mother cell (Nogler, 1984; Asker and Jerling, 1992). 26, 113–123. For example in Drosophila parthenogenetica, a small proportion of eggs laid by virgin females develop to produce viable adults. It functions normally in di-haploid egg cells, and is able to induce embryogenesis in aneuploid eggs, although, with early embryo abortion. doi: 10.1007/s00441-015-2291-8, Maheshwari, P. (1950). Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. Transcriptomes of isolated Oryza sativa gametes characterized by deep sequencing: evidence for distinct sex-dependent chromatin and epigenetic states before fertilization. Embryos arrest at an early stage in these mutants, and this may also involve failure of the endosperm, since they can be rescued by in vitro cultivation. This gene is related to the tumor suppressor gene RB in mammals, which has a role in inhibiting cell cycle progression. 290, 998–1009. doi: 10.1242/dev.102103, Schön, I., Martens, K., and van Dijk, P. J. examples of rare parthenogenesis in. Parthenogenesis involves the development of embryos from unfertilized eggs. doi: 10.1016/j.devcel.2017.10.005, Anderson, S. N., Johnson, C. S., Jones, D. S., Conrad, L. J., Gou, X., Russell, S. D., et al. I. Unraveling this changes in more detail may give clues for parthenogenetic reproduction. Breed. Front. doi: 10.1038/nature08828, Ortiz, J. P., Quarin, C. L., Pessino, S. C., Acuña, C., Martínez, E. J., Espinoza, F., et al. RBR1 represses the G1/S-phase transition through inhibiting E2F transcription, and this, in turn, involves RBR1-phosphorylation that influences the RBR1-E2F interaction (Boniotti and Gutierrez, 2001; Kuwabara and Gruissem, 2014). Restoring endosperm development is, therefore, necessary for successful seed development via parthenogenesis. doi: 10.1016/j.cub.2005.02.066, Hand, M. L., de Vries, S., and Koltunow, A. M. (2016). (1970). Bot. Alternatively, the egg cells in apomicts bypass a chromatin repressive and transcriptionally silent state and need reprogramming. doi: 10.1007/BF00229382, Mercier, R., Vezon, D., Bullier, E., Motamayor, J. C., Sellier, A., Lefèvre, F., et al. It sometimes occurs in lower plants as well. In rice and maize egg cells, TFs are also over-represented, as are genes involved in transcriptional regulation and nucleic acid binding (Anderson et al., 2013; Chen et al., 2017). Blacktip sharks are quite common in the coastal subtropical and tropical waters on the planet. 379, 633–646. Development 129, 3935–3943. (2007). Murbeck, S. (1904). 1669, 17–34. Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. *Correspondence: Kitty Vijverberg,, Front. Although successful in particular species or genotypes, others can be completely recalcitrant to produce DHs. Apparently, parthenogenesis can act in an aneuploid context, although with early embryo arrest. Indeed, studies that focused on specific invertebrate groups found high frequencies of parthenogenesis, for example it was found in 15% of Megastigmus (Boivin et al. Apomixis: developmental characteristics and genetics. Nature 428, 860–864. Appl. The FIS-class genes FIS2 and MEA are imprinted genes. All tetraploid and some triploid hybrids showed spontaneous seed formation, thus displaying all apomixis elements. Boca Raton FL: CRC Press. PLoS Biol. Depending on the mechanism involved, true or partial clones of the mother are produced. Copyright © 2019 Vijverberg, Ozias-Akins and Schranz. PLoS Genet. Parthenogenesis definition, development of an egg without fertilization. (2001). Until the recent findings of PsASGR-BBML and RKD-TFs, a candidate for parthenogenesis in plants mentioned in literature was the FIS-PRC2 gene MSI1 (Köhler et al., 2003a; Guitton and Berger, 2005; section “Egg Cell Arrest and the Trigger for Embryogenesis”). Identification and analysis of DYAD: a gene required for meiotic chromosome organisation and female meiotic progression in Arabidopsis. Ozias-Akins, P. (2006). 5:4645. doi: 10.1038/ncomms5645, d’Erfurth, I., Jolivet, S., Froger, N., Catrice, O., Novatchkova, M., and Mercier, R. (2009). Sci. Plant Reprod. However, in nature there are examples of the immaculate conception, and we are not only talking about single-cell organisms. The process of double fertilization in which the egg cell and central cell each are fertilized by one of two clonal sperm cells is unique to flowering plants (see for a review, e.g., Dresselhaus et al., 2016). This is known as facultative parthenogenesis. von Siebold, C. T. E. (1856). This process lacks the development of an embryo sac, endosperm, and seed coat. Cloning plants by seeds: Inheritance models and candidate genes to increase fundamental knowledge for engineering apomixis in sexual crops. They are seen as dark brown or gray lizards with a pale-translucent color at night and some light markings during the day. Natl. A transcriptional view on somatic embryogenesis. Apomictic species may thus have become independent from the FIS-PRC2, either because it has a (relatively) modified expression or they evolved changed requirements for it. doi: 10.1016/j.cub.2016.05.028, Sakuma, Y., Liu, Q., Dubouzet, J. G., Abe, H., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2002). II. These efforts have started to pay off, particularly by the isolation of the PsASGR-BabyBoom-Like from apomictic Pennisetum, a gene proven to be transferable to and functional in sexual pearl millet, rice, and maize. doi: 10.1080/07352680600563926, Pillot, M., Baroux, C., Vazquez, M. A., Autran, D., Leblanc, O., Vielle-Calzada, J. P., et al. Fertilization-independent seed development in Arabidopsis thaliana. Role of small RNAs in epigenetic reprogramming during plant sexual reproduction. It was suggested to be the result of a genetic load associated to long-term asexual reproduction that becomes apparent and lethal in haploid gametes. doi: 10.1007/s00497-001-0116-2, Anderson, S. N., Johnson, C. S., Chesnut, J., Jones, D. S., Khanday, I., Woodhouse, M., et al. 65, 2667–2676. “Wheat haploids through the Salmon method,” in Biotechnology Agriculture Forestry, Vol. Parthenogenese bei den Gattungen Taraxacum und Hieracium. Table 1. Mogie, M. (1992). Dosage-sensitive function of retinoblastoma related and convergent epigenetic control are required during the Arabidopsis life cycle. Bot. In apomictic parthenogenesis, common in plants, the diploid germ line cells (gametocytes) do not undergo meiosis to create gametes but rather undergo regular cell division, or mitosis; offspring are clones of the mother. doi: 10.1126/science.280.5362.446, Grossniklaus, U. Belogradova, K., Lewicka, I., Heberle-Bors, E., and Touraev, A. Although successful in a range of species, many species or particular genotypes can be (very) recalcitrant to in vitro embryogenesis and unable to produce embryos with any of the known stimuli (Ochatt et al., 2010; Soliìs-Ramos et al., 2012). In some parthenogenetic organisms of other kingdoms, such as insects, stimuli imparted to the egg cell during ovulation or egg-laying, or non-sperm-based signals, e.g., a change in ionic strength or pH, can trigger egg cell activation (Horner and Wolfner, 2008). It was hypothesized that the silencing of maternal alleles might have become reduced or relieved during the evolution of apomixis, allowing maternally imprinted genes to be expressed from the maternal allele. Parthenogenesis usually occurs in combination with a mechanism that keeps or restores the diploid chromosome number, since haploid offspring are usually less fit or non-viable in nature. Identifying a gene that is able to induce parthenogenesis particularly in these recalcitrant species and genotypes would be very valuable as a tool in plant breeding. They are silenced throughout the life cycle of the plant, but become active in the female gametophyte, especially in the central cell, and remain expressed and active in the endosperm after fertilization, whereas the paternal alleles remain silent (Wang and Köhler, 2017). And activate transcription and the replication machinery context of parthenogenesis in sexual species... 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